Structure-function analysis of the maize bulliform cell cuticle and its potential role in dehydration and leaf...

The hydrophobic cuticle of plant shoots serves as an important interaction interface with the environment. It consists of the lipid polymer cutin, embedded with and covered by waxes, and provides protection against stresses including desiccation, UV radiation, and pathogen attack. Bulliform cells form in longitudinal strips on the adaxial leaf surface, and have been implicated in the leaf rolling response observed in drought-stressed grass leaves. In this study, we show that bulliform cells of the adult maize leaf epidermis have a specialized cuticle, and we investigate its function along with that of bulliform cells themselves. Bulliform cells displayed increased shrinkage compared to other epidermal cell types during dehydration of the leaf, providing a potential mechanism to facilitate leaf rolling. Analysis of natural variation was used to relate bulliform strip patterning to leaf rolling rate, providing further evidence of a role for bulliform cells in leaf rolling. Bulliform cell cuticles showed a distinct ultrastructure with increased cuticle thickness compared to other leaf epidermal cells. Comparisons of cuticular conductance between adaxial and abaxial leaf surfaces, and between bulliform-enriched mutants versus wild-type siblings, showed a correlation between elevated water loss rates and presence or increased density of bulliform cells, suggesting that bulliform cuticles are more water-permeable. Biochemical analysis revealed altered cutin composition and increased cutin monomer content in bulliform-enriched tissues. In particular, our findings suggest that an increase in 9,10-epoxy-18-hydroxyoctadecanoic acid content, and a lower proportion of ferulate, are characteristics of bulliform cuticles. We hypothesize that elevated water permeability of the bulliform cell cuticle contributes to the differential shrinkage of these cells during leaf dehydration, thereby facilitating the function of bulliform cells in stress-induced leaf rolling observed in grasses.